Onderstepoort Journal of Veterinary Research, 60:95-101 (1993)

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ABSTRACT LOUW, J.P., HORAK, I.G. & BRAACK, L.E.O. 1993. Fleas and lice on scrub hares (Lepus saxatilis) in South Africa. Onderstepoort Journal of Veterinary Research, 60:95-101 (1993) A total of 380 scrub hares (Lepus saxatilis) from 5 localities, ranging from the north-eastern Transvaal to the eastern and the south-western Cape Province of South Africa, were examined for fleas and lice. Ctenocephalides felis damarensis was almost exclusively responsible for the flea infestations on hares at 4 of the 5 sites. At 4 localities the prevalence and abundance of this flea reached peaks between August and October and declined thereafter to their lowest levels between February and April. Its pre­ valence and abundance in the north-eastern Transvaal were not correlated with the breeding cycle of the hares in this region. The 2 louse species recovered, sometimes sympatrically, were Haemodipsus lyriocephalus and Haemodipsus setoni. Listrophorus leporicolus was the only mite species recovered.

INTRODUCTION tion maps for some species. The identity of the louse recovered from a scrub hare in South Africa Scrub hares (Lepus saxatilis) are widely distributed and described by Bedford (1934) as Haemodipsus in the Republic of South Africa and are particularly africanus has been disputed by other authors, who abundant in the eastern regions (Robinson 1982). state that the lice on these animals are either Hae­ In this country they are hosts of a number of flea modipsus ventricosus or Haemodipsus setoni (Led­ species (De Meillon, Davis & Hardy 1961; Haesel­ ger 1980). barth, Segerman & Zumpt 1966), lice (Ledger 1980) and ixodid ticks (Walker 1991). From 1983-1992, I.G. Horak regularly collected ectoparasites from scrub hares in various regions of The prevalence and seasonal abundance of various South Africa. The identity, monthly or bimonthly pre­ tick species on these hares in South Africa are well valence and abundance of their fleas and the iden­ documented (Horak, Sheppey, Knight & Beuthin tity and abundance of their lice are reported in this 1986; Rechav, Zeederberg & Zeller 1987; Horak & Fourie 1991) and the geographic distributions of paper. Similar data for their ticks have been pub­ lished separately (Horak et at. 1986; Horak, Fourie, several species have been plotted (Howell, Walker & Nevill 1978). There are no published data on the Novellie & Williams 1991; Horak & Fourie 1991). abundance of fleas on scrub hares in this country, but De Meillon et at. (1961) have provided distribu- MATERIALS AND METHODS Scrub hares sampled from 5 localities (Table 1) were processed for ectoparasite recovery as described by 1 Department of Parasitology, Faculty of Veterinary Science, University of Pretoria, Onderstepoort, 0110 South Africa Horak et a/. (1986) and Horak & Fourie (1991). 2 National Parks Board, Private Bag X402, Skukuza, 1350 South Fleas were mounted in lactophenol, left for a few Africa hours to clear and examined with a standard micro­ Received 16 February 1993- Editor scope. They were identified according to descriptions

95 Fleas and lice on scrub hares (Lepus saxatilis) in South Africa

TABLE 1 The localities at which scrub hares were collected, the duration of the collection periods and the numbers of scrub hares examined in South Africa

Number of hares Total Veld type Collection Collection Locality Coordinates collected number (Acocks 1988) period inteNals on each of hares occasion

North-eastern Transvaal

Shingwedzi 23°08'S, Mopani Veld June 1989- Bimonthly 3 18 31 °27'E Apr1990

Skukuza 24°58'S, Lowveld Aug 1988- Monthly· 5 240 31 °36'E July 1992

Eastern Cape Province

Mountain Zebra 32°15'S, Karroid Merxmeullera Feb 1983- 1-4 months 2 26 National Park 25°27'E Mountain Veld Dec 1985 replaced by Karoo

"Bucklands" a 33°05'8 , 26°40'E } Valley Bushveld Feb 1985- Monthly 4b 87 Andries Vosloo Kudu 33°08'S, Jan 1987 ReseNe a 26°40'E

South-western Cape Province

Bontebok National Park 34°02'S, Coastal Apr1983- Bimonthly 2b 11 20°25'E Renosterbosveld Feb 1984 a These properties share a common ± 11 km boundary b It was not possible to collect the required number of hares on each occasion by De Meillon et a/. (1961) and Haeselbarth et a/. Monthly mean maximum and minimum atmospheric (1966). Lice were placed on filter paper, allowed to temperatures and the total monthly rainfall were al­ dry and examined using a stereoscopic microscope so recorded at Skukuza. capable of 75 x magnification. The descriptions of Ferris (1932) were used to identify the lice. In order to confirm the identifications made under the stereo­ RESULTS scopic microscope, a single male and female of each species were examined under a scanning elec­ The numbers of fleas and lice recovered from the tron microscope. hares and the prevalence of infestation are summa­ rized in Table 2. The mean numbers of fleas recovered from the scrub hares were plotted to depict seasonal and Four species of fleas and 2 species of lice were re­ relative abundance, while the percentage of animals covered. Ctenocephalides felis damarensis was the infested on each occasion represents the prevalen­ most abundant find widely distributed flea, while ce of infestation. Haemodipsus lyriocephalus was the most abundant and H. setoni the most widely distributed louse. The numbers of scrub hares that were either preg­ nant or lactating were recorded during the survey at The seasonal abundances and prevalences of fleas Skukuza. On completion of the survey, the mean cu­ on the hares examined at Shingwedzi, Skukuza, mulative percentage of pregnant or lactating hares Mountain Zebra National Park, "Bucklands" combin­ was calculated for each calendar month and plotted ed with the Andries Vosloo Kudu Reserve, and the to represent the mean monthly reproductive status Bontebok National Park are graphically presented in of the animals. Fig. 1- 5 respectively.

96 J.P. LOUW, I.G. HORAK and L.E.O. BRAACK

TABLE 2 The total number of fleas and lice recovered from scrub hares examined at various localities in South Africa

No. of Ctenocephalides felis damarensis Echidnophaga spp. Haemodipsus spp. scrub Localities hares exam- E. galli- E. Ia- H. lyrio- d' ~ X Total H. setoni ined nacea rina cephalus

Shingwedzi 18 241 307 0 548 (14) 0 0 0 0 Skukuza 240 575 839 140 1554 (183) 0 3 (3) 343 (8) 126 (23) Mountain Zebra Park 26 55 76 0 131 (18) 3 (3) 0 0 1 (1 ) Bucklands & Kudu Reserve 87 588 851 0 1439 (74) 166 (4) 0 0 0 Bontebok National Park 11 a -- - 36 (7) 1 (1) 0 0 41 (5)

X number of fleas damaged and impossible to determine species or sex ( ) number of hares infested a 1 hare infested with Dinopsyllus sp.

At Shingwedzi the largest number of fleas was re­ were the lowest. Echidnophaga gal/inacea, a flea of corded during August; at Skukuza this peak occur­ domestic fowls, was occasionally found, but signifi­ red during September 1988 & 1990 and during Oc­ cant numbers were recovered only once, namely in tober 1989 & 1991. No pattern of seasonal abun­ the Andries Vosloo Kudu Reserve in August 1986 dance was obvious for the fleas recovered in the (Fig. 4). The fairly large numbers present on this Mountain Zebra National Park, while peak burdens occasion suggest that the particular hares involved were recorded during October 1985 on "Bucklands" must have acquired the infestation near human ha­ combined with the Andries Vosloo Kudu Reserve, bitation. A few Echidnophaga Iarina, a common flea and August in the Bontebok National Park. of warthogs (Horak, Boomker, De Vas & Potgieter 1988), were present on 3 hares at Skukuza. A single The mean monthly percentage of hares at Skukuza specimen of a Dinopsyllus sp., a flea usually associ­ that were pregnant or lactating, or both, is graphi­ ated with rodents, was recovered from a hare in the cally illustrated in Fig. 6. Breeding appeared to take Bontebok National Park. These aberrant infestations place throughout the year with no clear indication of probably occurred as a result of intrusion or sharing a seasonal peak. of the habitat by the various hosts and is a common Atmospheric temperatures and total monthly rainfall phenomenon (Avetisyan & Ezekelyan 1975). In Ken­ at Skukuza are graphically presented in Fig. 7. ya Flux (1972) found that Lepus capensis was most commonly infested with Ctenocephalides felis stron­ The highest maximum temperatures were generally gylus and to a lesser extent by E. gallinacea. recorded during January and February. Most rain usually fell from November or December to January In South Africa C. felis damarensis has long been or February. recognized as the sole representative of this genus parasitizing scrub hares (De Me ilion et a/. 1961). The difference in the shape of the sternal plates of These authors, however, questioned the status of the 2 louse species as well as the presence of dis­ this flea as a subspecies of C. felis and felt that it tinct sclerotized paratergites protruding from the lat­ should be named C. damarensis, a species in its eral borders of abdominal segments 3-6 of H. seto­ own right. The present study confirms that C. felis ni, compared to mere sclerotized points in H. lyrio­ damarensis is a successful parasite of scrub hares cephalus, are evident from Fig. 8 & 9. and is established throughout the country. Listrophorus leporicolus was the only mite recover­ For its reproduction, Spilopsyl/us cuniculi, the Euro­ ed from the scrub hares in the present study. pean rabbit flea, is entirely dependent upon the ste­ roid hormones circulating in pregnant does (Mead­ DISCUSSION Briggs 1964). Rothschild & Ford (1972) found that Fleas the ovaries of female Cediopsyl/a simplex, a flea infesting rabbits and hares in North America, only A single species, C. felis damarensis, was respon­ developed when the flea fed on either pregnant sible for almost all flea infestations on the scrub does or newborn rabbits. Feeding on oestrous does hares. The largest populations were found on hares caused a resorption of all developing oocytes and at Shingwedzi in the north of the country, while a rapid regression of the ovaries of the female fleas. those in the Bontebok National Park in the south Thus the breeding cycles of these flea species are

97 Fleas and lice on scrub hares (Lepus saxatilis) in South Africa

Mean number of Prevalence of Mean number of Prevalence of fleas (n = 3) infestation (%) fleas (n = 2) infestation (%) 120 120 20 -r--=-.:...._---'------'--,- 120 llllillilll Fleas + % Hares infested llliiiiiiiFieas+ % Hares infested 100 100 100

80 80 80

60 60 60

40 40 40

20 20 20

0 0 0 MAONFMANMJ SO J A 0 D F A 1983 1984 I 1985 1989 1990 FIG. 1 The seasonal abundance and prevalence of Ctenoce­ FIG. 3 The abundance and prevalence of Ctenocephalides phalides felis damarensis on scrub hares around Shing­ felis damarensis on scrub hares in the Mountain Zebra wedzi, Kruger National Park, north-eastern Transvaal National Park, eastern Cape Province

Mean number of Prevalence of Mean number of Prevalence of fleas (n 5) infestation(%) fleas (n = 4) infestation (%) = 100 .....------.,- 120 120 lllillllll Ctenocephalides • Echidnophaga * % Hares infested 100 80 30 80 60 20 60 40 40 10 20 20

0 1988 I 1989 1990 1991 I 1992 FIG. 2 The seasonal abundance and prevalence of Ctenoce­ FIG. 4 The seasonal abundance and prevalence of Ctenoce­ phalides felis damarensis on scrub hares around Sku­ phalides felis damarensis on scrub hares on the farm kuza, Kruger National Park, north-eastern Transvaal "Bucklands" combined with the Andries Vosloo Kudu Reserve, eastern Cape Province

synchronized with the arrival of the leverets, which 5). This occurred in the sub-tropical north-eastern they then infest. Transvaal, the hot and fairly dry Valley Bushveld of the eastern Cape Province and the Mediterranean In the present study there was no evidence of an increase in the numbers of C. felis damarensis on climatic zone in the south-western Cape Province. pregnant or lactating females. During the period At Skukuza the increase in flea numbers coincided February- April, when all female scrub hares exam­ with an increase fn temperature at a time when ined at Skukuza were either pregnant or lactating there was little or no rain (Fig. 2 & 7). In the Moun­ (Fig. 6), both the prevalence and abundance of flea tain Zebra National Park, however, the numbers of infestations on the hares sampled at this locality fleas seemed to reach a peak in autumn (Fig. 3). were at their lowest (Fig. 2). However, in the lactat­ This region differs from the others in that minimum ing females the reason for this might have been winter temperatures are considerably lower and that that their flea populations had transferred to the snowfalls may occur in winter and spring. newborn leverets. The abundance and prevalence of C. felis damarensis increased during mid- to late Cooke (1984) and Cooke & Skewes (1988) showed winter, reached a peak in August to October and that survival of the larvae and adults of the Euro­ then declined at 4 of the 5 localities (Fig. 1, 2, 4 & pean rabbit flea, S. cuniculi, was seriously affected

98 J.P. LOUW, I.G. HORAK and L.E.O. BRAACK

Mean number of Prevalence of 300 40 fleas (n = 2) infestation (%) 10 120 IIIIIIIIIIIIFieas+ % Hares infested 225 100 "E 8 .s ~ 150 80 c "iii 6 a: 60 75 4 40 0 O AODFAJAODFAJAODFAJAODFAJ 2 1988/891--lmf97!1o~r99W!f1-rf9!r179Zl 20 FIG. 7 Mean maximum and minimum atmospheric tempera­ tures and total monthly rainfall at Skukuza from August 0 0 Apr Jun Aug Oct Dec Feb 1988-July 1992 1983 1984 50%. The low numbers of fleas and low prevalen­ FIG. 5 The seasonal abundance and prevalence of Ctenoce­ ces of infestation recorded during the hot summer phalides felis damarensis on scrub hares in the Bonte­ bok National Park, south-western Cape Province and early autumn months at nearly all localities in the present survey indicate that high temperature, rather than low humidity, is probably a more impor­ tant climatic factor limiting flea infestations on scrub % n 120 -,------==------,- 14 hares. Most rain generally fell during the period No­ ...... Pregnant / lactating % llill Females e~amined (n) vember- February, but these also include the hottest 100 - months (Fig. 7). According to Smithers (1983) scrub hares may 80 - return to the same form for a number of days. The seasonal abundance of C. felis damarensis re­ 60 - corded in the present survey suggests that the '- 6 same form or its vicinity may be used either regular­ 40 - ly or erratically for a period of 2- 3 months from I- 4 June or July to September or October. This would 20 - I- 2 not only allow the flea's life cycle to be completed, but also enable numbers to increase. It could 0 - '-- 0 equally imply that the same form, or the vicinity of JFMAMJJASOND the same form, is inhabited annually during these Months of year months. Fleas that had oversummered as pupae in FIG. 6 Monthly reproductive status of female scrub hares the latter forms would then be immediately available around Skukuza, Kruger National Park, north-eastern to infest the hares inhabiting these structures during Transvaal mid-winter to spring. Horak (1982) found that once Ctenocephalides spp. by high temperatures, especially when conditions of had become established in a dog kennel in Pretoria low humidity prevailed. However, the eggs and North, in the central Transvaal, burdens rose rapidly pupae of this flea were more resistant to adverse in November-January and remained at a high level climatic conditions and these authors postulated until approximately May. He ascribed this increase that fleas might persist in the rabbit warrens through to a rise in humidity subsequent to substantial rain­ the summer months as quiescent pupae. fall during October, rather than temperature which The fact that the seasonal pattern of flea infestation had already started to climb in August. In Cairo, was similar at all but 1 of the localities in the pres­ Amin (1966) recorded 2 periods of peak abundance ent survey, regardless of whether these were situ­ of Ctenocephalides felis felis on dogs. The 1st in ated in winter or summer rainfall zones, indicates spring followed an increase in temperature after that humidity may not play a definitive role in the winter; the other in autumn followed a rise in rela­ life-cycle of C. felis damarensis. Cooke (1990) tive humidity after the dry summer. showed that fleas in the wild are adapted to condi­ tions of low humidity. For instance Xenopsylla cuni­ Lice cularis, the flea of the wild European rabbit, Orycto­ Ferris (1932) listed 3 species of lice of the genus lagus cuniculus, can survive at relative humidities of Haemodipsus from the Leporidae, namely H. lyrio-

99 Fleas and lice on scrub hares (Lepus saxatilis) in South Africa

FIG. 9 Scanning electron micrograph of Haemodipsus setoni (x 70) FIG. 8 Scanning electron micrograph of Haemodipsus lyrioce­ phalus (x 70) cephalus, H. setoni and H. ventricosus. Bedford Kudu Reserve and on the farm "Bucklands" respec­ (1934) described a 4th species, H. africanus, from tively. a hare in South Africa. This species was based on Mrs S. Meyer and Miss M.L. Horak of the University a single female and has never been recorded since, of Pretoria and Mr E.J. Williams of Rhodes Univer­ nor can the type specimen be found for compari­ sity assisted with the recovery of the parasites from son. Subsequent to Bedford's finding, Kim & Emer­ the processed material. son (1970, cited by Ledger 1980) recorded collec­ tions of H. ventricosus from L. capensis in this coun­ Mr Leon Limper of the Onderstepoort Veterinary In­ try. stitute is thanked for the scanning electron micro­ graphs of the lice, Mrs A. Lubbe for typing the man­ In the present study only H. lyriocepha/us and H. uscript and Miss A. van Niekerk for drawing the setoni were found on the scrub hares. The 2 occur­ climatic graph. red sympatrically at Skukuza, while only H. setoni was present on the hares in the Bontebok National This research was funded by the Foundation for Park. Two scrub hares collected at Vanrhynsdorp, Research Development, the South African Nature near the west coast of South Africa, were also in­ Foundation and Bayer Animal Health. fested only with H. setoni. REFERENCES ACKNOWLEDGEMENTS AM IN, O.M. 1966. The fleas (Siphonaptera) of Egypt: distribution and seasonal dynamics of fleas infesting dogs in the Nile This study is part of the Wildlife Research Program­ Valley and Delta. Journal of Medical Entomology, 3:293- 298. me of the Faculty of Veterinary Science, University AVETISYAN, G.A. & EZEKELYAN, V. Kh. 1975. Fleas of certain of Pretoria. species of rodents in Armenia. 1. Biologicheskii-Zhurnai-Arme­ nii, 28:56-63. We wish to express our thanks to the National BEDFORD, G.A.H. 1934. Descriptions of new species of Anoplu­ Parks Board of Trustees, who made available scrub ra parasitic on antelopes and a hare. Onderstepoort Journal hares in the Kruger, Bontebok and Mountain Zebra of Veterinary Science and Anima/Industry, 2:41-48. National Parks. The Division of Nature Conservation COOKE, B.D. 1984. Factors limiting the distribution of the rabbit of the Cape Provincial Administration and Mr W. A. flea, Spilopsyllus cuniculi (Dale) (Siphonaptera), in inland Phillips provided the animals in the Andries Vosloo South Australia. Australian Journal of Zoology, 32:493- 506.

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